Modeling the effect of stretch and plasma membrane tension on Na +-K+-ATPase activity in alveolar epithelial cells

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 292, Issue 1, 2007, Pages

  Fisher, Jacob L ^a   Margulies, Susan S ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Edema recovery; Lipid trafficking; Ventilator induced lung injury

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); MEMBRANE LIPID;

ARTICLE; ARTIFICIAL VENTILATION; CELL DAMAGE; CELL MEMBRANE; CELL VIABILITY; ENZYME ACTIVITY; LUNG ALVEOLUS EPITHELIUM; MATHEMATICAL MODEL; PRIORITY JOURNAL; STRETCH RECEPTOR; TENSION; VALIDITY;

ANIMALS; CELL MEMBRANE; CELLS, CULTURED; ELASTICITY; EPITHELIAL CELLS; MEMBRANE LIPIDS; MODELS, BIOLOGICAL; NA(+)-K(+)-EXCHANGING ATPASE; POSITIVE-PRESSURE RESPIRATION; PULMONARY ALVEOLI; RATS; RESPIRATORY MECHANICS; STRESS, MECHANICAL;

EID: 33846204373     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00425.2005     Document Type: Article

References (65)

1. Baldwin DN, Suki B, Pillow JJ, Roiha HL, Minocchieri S, and Frey U. Effect of sighs on breathing memory and dynamics in healthy infants. J Appl Physiol 97: 1830-1839, 2004.
2. Berrios JC and Hubmayr RD. Deforming stress triggers endocytosis in alveolar epithelial cells (Abstract). Am J Respir Crit Care Med 167: A57, 2003.
3. Brower RG, Lanken PN, MacIntyre N, Matthay MA, Morris A, Ancukiewicz M, Schoenfeld D, and Thompson BT. Higher versus lower positive end-expiratory pressures in patients with the acute respiratory distress syndrome. N Engl J Med 351: 327-336, 2004.
4. Chen CS and Ingber DE. Tensegrity and mechanoregulation: from skeleton to cytoskeleton. Osteoarthritis Cartilage 7: 81-94, 1999.
5. Dai J and Sheetz MP. Cell membrane mechanics. Methods Cell Biol 55: 157-171, 1998.
6. Dai J and Sheetz MP. Regulation of endocytosis, exocytosis, and shape by membrane tension. Cold Spring Harb Symp Quant Biol 60: 567-571, 1995.
7. Dai J, Sheetz MP, Wan X, and Morris CE. Membrane tension in swelling and shrinking molluscan neurons. J Neurosci 18: 6681-6692, 1998.
8. Dai J, Ting-Beall HP, and Sheetz MP. The secretion-coupled endocytosis correlates with membrane tension changes. J Gen Physiol 110: 1-10, 1997.
9. Dong C and Skalak R. Leukocyte deformability: finite element modeling of large viscoelastic deformation. J Theor Biol 158: 173-193, 1992.
10. Dong C, Skalak R, and Sung KL. Cytoplasmic rheology of passive neutrophils. Biorheology 28: 557-567, 1991.
11. Dong C, Skalak R, Sung KL, Schmid-Schonbein GW, and Chien S. Passive deformation analysis of human leukocytes. J Biomech Eng 110: 27-36, 1988.
12. Dos Santos CC and Slutsky AS. Mechanisms of ventilator-induced lung injury: a perspective. Invited Review. J Appl Physiol 89: 1645-1655, 2000.
13. Dreyfuss D and Saumon G. Role of tidal volume, FRC, and endinspiratory volume in the development of pulmonary edema following mechanical ventilation. Am Rev Respir Dis 148: 1194-1203, 1993.
14. Dreyfuss D and Saumon G. Ventilator-induced lung injury: lessons from experimental studies. Am J Respir Crit Care Med 157: 294-323, 1998.
15. Dreyfuss D, Soler P, Basset G, and Saumon G. High inflation pressure pulmonary edema. Respective effects of high airway pressure, high tidal volume, and positive end-expiratory pressure. Am Rev Respir Dis 137: 1159-1164, 1988.
16. +-ATPase activation during alveolar epithelial stretch (Doctoral Thesis). Philadelphia, PA: University of Pennsylvania, 2004.
17. Fisher JL, Levitan I, and Margulies SS. Changes in alveolar epithelial cell plasma membrane surface area with static stretch. 2003 Summer Bioengineering Conference of the ASME Bioengineering Division, Key Biscayne, Florida, 2003.
18. Fisher JL, Levitan I, and Margulies SS. Plasma membrane surface increases with tonic stretch of alveolar epithelial cells. Am J Respir Cell Mol Biol 31: 200-208, 2004.
19. +-ATPase activity in alveolar epithelial cells increases with cyclic stretch. Am J Physiol Lung Cell Mol Physiol 283: L737-L746, 2002.
20. Forgacs G. On the possible role of cytoskeletal filamentous networks in intracellular signaling: an approach based on percolation. J Cell Sci 108: 2131-2143, 1995.
21. Gajic O, Lee J, Doerr CH, Berrios JC, Myers JL, and Hubmayr RD. Ventilator-induced cell wounding and repair in the intact lung. Am J Respir Crit Care Med 167: 1057-1063, 2003.
22. Hamill OP and Martinac B. Molecular basis of mechanotransduction in living cells. Physiol Rev 81: 685-740, 2001.
23. Hao M and Maxfield FR. Characterization of rapid membrane internalization and recycling. J Biol Chem 275: 15279-15286, 2000.
24. Hase CC, Le Dain AC, and Martinac B. Purification and functional reconstitution of the recombinant large mechanosensitive ion channel (MscL) of Escherichia coli. J Biol Chem 270: 18329-18334, 1995.
25. Hochmuth FM, Shao JY, Dai J, and Sheetz MP. Deformation and flow of membrane into tethers extracted from neuronal growth cones. Biophys J 70: 358-369, 1996.
26. Hochmuth RM. Cell biomechanics: a brief overview. J Biomech Eng 112: 233-234, 1990.
27. Hochmuth RM. Micropipette aspiration of living cells. J Biomech 33: 15-22, 2000.
28. Ingber DE, Dike L, Hansen L, Karp S, Liley H, Maniotis A, McNamee H, Mooney D, Plopper G, Sims J, and et al. Cellular tensegrity: exploring how mechanical changes in the cytoskeleton regulate cell growth, migration, and tissue pattern during morphogenesis. Int Rev Cytol 150: 173-224, 1994.
29. Kloda A and Martinac B. Structural and functional differences between two homologous mechanosensitive channels of Methanococcus jannaschii. EMBO J 20: 1888-1896, 2001.
30. Le Dain AC, Saint N, Kloda A, Ghazi A, and Martinac B. Mechanosensitive ion channels of the archaeon Haloferax volcanii. J Biol Chem 273: 12116-12119, 1998.
31. Lewis SA and de Moura JL. Incorporation of cytoplasmic vesicles into apical membrane of mammalian urinary bladder epithelium. Nature 297: 685-688, 1982.
32. Markin VS and Martinac B. Mechanosensitive ion channels as reporters of bilayer expansion. A theoretical model. Biophys J 60: 1120-1127, 1991.
33. Mills LR and Morris CE. Neuronal plasma membrane dynamics evoked by osmomechanical perturbations. J Membr Biol 166: 223-235, 1998.
34. Morris CE and Homann U. Cell surface area regulation and membrane tension. J Membr Biol 179: 79-102, 2001.
35. Morris CE, Lesiuk H, and Mills LR. How do neurons monitor their mechanical status? Biol Bull 192: 118-120, 1997.
36. Mutch WA, Harms S, Ruth Graham M, Kowalski SE, Girling LG, and Lefevre GR. Biologically variable or naturally noisy mechanical ventilation recruits atelectatic lung. Am J Respir Crit Care Med 162: 319-323, 2000.
37. Needham D and Hochmuth RM. A sensitive measure of surface stress in the resting neutrophil. Biophys J 61: 1664-1670, 1992.
38. Priebe GP and Arnold JH. High-frequency oscillatory ventilation in pediatric patients. Respir Care Clin N Am 7: 633-645, 2001.
39. Raucher D and Sheetz MP. Characteristics of a membrane reservoir buffering membrane tension. Biophys J 77: 1992-2002, 1999.
40. Ritacca FV and Stewart TE. Clinical review: high-frequency oscillatory ventilation in adults - a review of the literature and practical applications. Crit Care 7: 385-390, 2003.
41. Sachs F and Morris CE. Mechanosensitive ion channels in nonspecialized cells. Rev Physiol Biochem Pharmacol 132: 1-77, 1998.
42. Satcher RL Jr and Dewey CF Jr. Theoretical estimates of mechanical properties of the endothelial cell cytoskeleton. Biophys J 71: 109-118, 1996.
43. Schneider SW. Kiss and run mechanism in exocytosis. J Membr Biol 181: 67-76, 2000.
44. Schreiber MD, Gin-Mestan K, Marks JD, Huo D, Lee G, and Srisuparp P. Inhaled nitric oxide in premature infants with the respiratory distress syndrome. N Engl J Med 349: 2099-2107, 2003.
45. Sheetz MP and Dai JW. Modulation of membrane dynamics and cell motility by membrane tension. Trends Cell Biol 6: 85-89, 1996.
46. Singh JM and Stewart TE. High-frequency oscillatory ventilation in adults with acute respiratory distress syndrome. Curr Opin Crit Care 9: 28-32, 2003.
47. Stamenovic D and Coughlin MF. The role of prestress and architecture of the cytoskeleton and deformability of cytoskeletal filaments in mechanics of adherent cells: a quantitative analysis. J Theor Biol 201: 63-74, 1999.
48. Stroetz RW, Vlahakis NE, Walters BJ, Schroeder MA, and Hubmayr RD. Validation of a new live cell strain system: characterization of plasma membrane stress failure. J Appl Physiol 90: 2361-2370., 2001.
49. Sukharev S. Purification of the small mechanosensitive channel of Escherichia coli (MscS): the subunit structure, conduction, and gating characteristics in liposomes. Biophys J 83: 290-298, 2002.
50. Tabarean IV and Morris CE. Membrane stretch accelerates activation and slow inactivation in Shaker channels with S3-S4 linker deletions. Biophys J 82: 2982-2994, 2002.
51. Tsai MA, Frank RS, and Waugh RE. Passive mechanical behavior of human neutrophils: effect of cytochalasin B. Biophys J 66: 2166-2172, 1994.
52. Tsai MA, Frank RS, and Waugh RE. Passive mechanical behavior of human neutrophils: power-law fluid. Biophys J 65: 2078-2088, 1993.
53. Tschumperlin DJ. Deformation and injury of the alveolar epithelium (Doctoral Thesis). Philadelphia: University of Pennsylvania, 1998.
54. Tschumperlin DJ and Margulies SS. Alveolar epithelial surface area-volume relationship in isolated rat lungs. J Appl Physiol 86: 2026-2033, 1999.
55. Tschumperlin DJ and Margulies SS. Equibiaxial deformation-induced injury of alveolar epithelial cells in vitro. Am J Physiol Lung Cell Mol Physiol 275: L1173-L1183, 1998.
56. Tschumperlin DJ, Oswari J, and Margulies SS. Deformation-induced injury of alveolar epithelial cells. Effect of frequency, duration, and amplitude. Am J Respir Crit Care Med 162: 357-362, 2000.
57. Vlahakis NE and Hubmayr RD. Invited review: plasma membrane stress failure in alveolar epithelial cells. J Appl Physiol 89: 2490-2496; discussion 2497, 2000.
58. Vlahakis NE and Hubmayr RD. Response of alveolar cells to mechanical stress. Curr Opin Crit Care 9: 2-8, 2003.
59. Vlahakis NE, Schroeder MA, Pagano RE, and Hubmayr RD. Deformation-induced lipid trafficking in alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol 280: L938-L946, 2001.
60. Vlahakis NE, Schroeder MA, Pagano RE, and Hubmayr RD. Role of deformation-induced lipid trafficking in the prevention of plasma membrane stress failure. Am J Respir Crit Care Med 166: 1282-1289, 2002.
61. Wan X, Harris JA, and Morris CE. Responses of neurons to extreme osmomechanical stress. J Membr Biol 145: 21-31, 1995.
62. West JB. Respiratory physiology: the essentials. Baltimore, MD: Williams & Wilkins, 1990.
63. Yeung A and Evans E. Cortical shell-liquid core model for passive flow of liquid-like spherical cells into micropipets. Biophys J 56: 139-149, 1989.
64. Zhelev DV, Needham D, and Hochmuth RM. Role of the membrane cortex in neutrophil deformation in small pipets. Biophys J 67: 696-705, 1994.
65. Zhu C, Bao G, and Wang N. Cell mechanics: mechanical response, cell adhesion, and molecular deformation. Annu Rev Biomed Eng 2: 189-226, 2000.